Dimorphism-dependent transgenerational effects facilitate divergence of drought tolerance in Synedrella nodiflora

Aims Transgenerational effects in plants incur opposing effects on the adaptation to predictable vs. unpredictable environments. While seed-dimorphic plants can produce dimorphic offspring with different adaptive strategies, it remains unclear whether the transgenerational effects and seed dimorphism may interact to dictate offspring adaptation. This study aimed to explore whether and how seed-dimorphic maternal plants impart different transgenerational effects to dimorphic offspring. Methods Synedrella nodiflora was chosen as a study species, which is adaptive to a wide soil water gradient and produces two distinctive types of seeds (light disc vs. heavy ray seeds). In a greenhouse, S. nodiflora was grown for two generations under drought stress to test whether the transgenerational effects on offspring performance and mortality depend on maternal or offspring seed morph. The potential regulatory mechanisms were explored by measuring seed provisioning and chemical regulators of maternal plants and related reproductive processes. Important Findings The transgenerational effects depended on both maternal and offspring seed morphs. Drought stress induced the maternal plants originated from ray seeds to increase the relative proportion of ray- vs. disc-seed offspring and transmit stronger adaptive transgenerational effects to the former, whereas its effects on the maternal plants originated from disc seeds were exactly opposite. These different effects on offspring corresponded with different seed abscisic acid and soluble sugar contents but not seed provisioning. Dimorphism-dependent transgenerational effects allow large divergence of drought tolerance among offspring, which may be an important but under-explored mechanism to balance the needs of population maintenance and range expansion in seed-dimorphic species.